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By Scleractinian Corals (Cnidaria: Anthozoa) RESEARCH ARTICLE Selective consumption of sacoglossan sea slugs (Mollusca: Gastropoda) by scleractinian corals (Cnidaria: Anthozoa) Rahul Mehrotra1,2, Coline Monchanin2, Chad M. Scott2, Niphon Phongsuwan3, 4,5 1,6 7 Manuel Caballer GutierrezID , Suchana ChavanichID *, Bert W. Hoeksema 1 Reef Biology Research Group, Department of Marine Science, Faculty of Science, Chulalongkorn University, Bangkok, Thailand, 2 New Heaven Reef Conservation Program, Koh Tao, Suratthani, Thailand, 3 Department of Marine and Coastal Resources, Bangkok, Thailand, 4 MuseÂum National d'Histoire a1111111111 Naturelle, Directions des Collections, Paris, France, 5 American University of Paris, Department of Computer a1111111111 Science Math and Environmental Science, Paris, France, 6 Center for Marine Biotechnology, Department of a1111111111 Marine Science, Faculty of Science, Chulalongkorn University, Bangkok, Thailand, 7 Taxonomy and a1111111111 Systematics Group, Naturalis Biodiversity Center, RA Leiden, The Netherlands a1111111111 * [email protected] Abstract OPEN ACCESS Recent studies revealed that reef corals can eat large-sized pelagic and benthic animals in Citation: Mehrotra R, Monchanin C, Scott CM, Phongsuwan N, Caballer Gutierrez M, Chavanich S, addition to small planktonic prey. As follow-up, we document natural ingestion of sea slugs et al. (2019) Selective consumption of sacoglossan by corals and investigate the role of sacoglossan sea slugs as possible prey items of scler- sea slugs (Mollusca: Gastropoda) by scleractinian actinian corals. Feeding trials were carried out using six sacoglossan species as prey, two corals (Cnidaria: Anthozoa). PLoS ONE 14(4): e0215063. https://doi.org/10.1371/journal. each from the genera Costasiella, Elysia and Plakobranchus, and four free-living solitary pone.0215063 corals (Danafungia scruposa, Fungia fungites, Pleuractis paumotensis and Heteropsammia Editor: Shashank Keshavmurthy, Biodiversity cochlea) as predators. Trials were carried out under both in-situ and ex-situ conditions with Research Center, TAIWAN the aim to observe ingestion and assess signs of prey consumption based on tissue loss of Received: October 2, 2018 prey individuals over time. Significant differences were observed in both ingestion time and consumption state of prey between prey species, with three of them being ingested more Accepted: March 19, 2019 rapidly and preferentially consumed over the others. Additionally, prey size was found to be Published: April 29, 2019 a significant factor with larger prey (>12 mm) being ingested more slowly and rarely than Copyright: © 2019 Mehrotra et al. This is an open smaller ones (<6 mm and 6±12 mm). Comparisons of consumption capability among preda- access article distributed under the terms of the tors showed no significant difference with all coral species showing similar preferences for Creative Commons Attribution License, which permits unrestricted use, distribution, and prey species. While no specific mechanism of prey capture is proposed, we also document reproduction in any medium, provided the original instances of kleptoparisitism and resuspension of prey items by wrasses. This study high- author and source are credited. lights the important distinction between opportunistic prey capture and true predation Data Availability Statement: All data used in the events. present study are included as a Supporting Information file and are openly accessible. Funding: RM received support from Conservation Diver (Registered US Charity #20183007707), http://conservationdiver.com/. RM received support from the Graduate School at Introduction Chulalongkorn University, https://www.chula.ac.th/ en/. SC received support from NRCT-JSPS Core to Sea slugs (Mollusca: Gastropoda: Heterobranchia) are more commonly known as predator Core, Thailand Research Fund (RSA 6080087), than as prey, which is largely attributed to the chemical defences acquired from their prey PLOS ONE | https://doi.org/10.1371/journal.pone.0215063 April 29, 2019 1 / 22 Consumption of sea slugs by scleractinian corals https://nrct.go.th/. SC received support from species [1±3]. Though less extensive, a growing number of instances of sea slugs as prey species TASCMAR EU Horizon 2020, http://www.tascmar. have been recorded, as part of in-situ observations and experiments, in particular with cnidar- eu/. NO. ian predators [4,5]. However, once a prey is captured, it is not sure that it will also be con- Competing interests: The authors have declared sumed because it may become released and eventually escape [6]. that no competing interests exist. Sacoglossans are a speciose clade of sea slugs that feed almost exclusively on algal matter [7]. A small number of sacoglossans species have been found to be predated upon by a variety of organisms including small fish, nemerteans, crustaceans, a scleractinian coral, and other sea slugs [5, 8±10]. These predatory organisms either display a high degree of tolerance to seques- tered toxins in prey species or are completely unaffected by them, with a few cases known of prey rejection due to sacoglossan toxins [2,8]. Heterotrophy in scleractinian reef corals plays a vital role in the growth of coral tissue, even though this usually plays an inferior role compared to energy acquisition through autotrophy [11,12]. Heterotrophy can meet 15±35% of daily metabolic requirements in healthy zoox- anthellate corals and up to 100% in bleached corals, and can account up to 66% of carbon used in their skeletons [12]. Key nutritional importance of heterotrophy has been reported to include acquisition of amino acids and nutrients such as nitrogen and phosphorus as these are not acquired by the coral via photosynthesis. Prey composition of scleractinian predators is composed largely of zooplankton and particulate organic matter (POM) of various sizes. Zoo- plankton prey include isopods, amphipods, crab larvae, copepods, nematodes, nemerteans, polychaetes, and jellyfish [13±17]. While the mechanics of prey digestion have received some attention, prey rejection in scler- actinian corals has not been studied in great detail. Studies into predation and dietary prefer- ences have been conducted for well over a century [18±20] with some sparse mention of prey rejection. Notably de Lecaze-Duthiers [18] documented ingestion and subsequent rejection of live whelks, Nucella lapillus, during feeding trials on the dendrophylliid coral Balanophyllia regia. Subsequent observations made on the subject include notes of `gut content discharge' [14] and the rejection of prey under varying conditions/stimuli [21±23]. In recent years, a growing number of observations have shown how large planktonic fauna such as salps and jellyfish may act as prey for corals [24±28]. These records suggest that gape size in corals directly limits the range of potential prey items [26]. Nearly all of the predatory corals observed so far, appear to be free-living, allowing them to live in various reef zones, including deeper sandy seafloors [29±31]. These free-living corals are mobile and can also shed sediments relative easily [32±34].The ability to survive on unconsolidated substrates enables free-living corals to expand the reef habitat by means of spreading their skeletons as hard pieces of substrate in downslope direction beyond the lower reef slope boundary in an ecological and evolutionary context [30,35,36]. A number of free-living zooxanthellate sclerac- tinian corals of various families are known to live almost exclusively in soft sediment non-reef habitats, such as Heteropsammia spp. (Dendrophylliidae), Heterocyathus spp. (Caryophyllii- dae), Cycloseris spp. (Fungiidae), and Goniopora stokesi (Poritidae) [30, 36±38]. There are also some free-living coral species without zooxanthellae that can thrive on sandy bottoms near reefs but usually live in much deeper and colder water, such as Truncatoflabellum spp. (Flabel- lidae) and Deltocyathoides spp. (Turbinoliidae) [39±41]. Little is known about the ecology of these low-cover, soft-bottom communities near reefs, which have been considered to play a limited role in reef-building [35]. It remains unclear whether the ability to survive in these hab- itats for these corals is linked to their gape size and thus, to their predatory capacity of larger prey items. Free-living corals of the species Heteropsammia cochlea and Pleuractis paumotensis were recently observed to ingest salps and a sea slug at Koh Tao, Gulf of Thailand [5,26]. The 19-km2 island is surrounded by a fringing coral reef, with many of the locations around the PLOS ONE | https://doi.org/10.1371/journal.pone.0215063 April 29, 2019 2 / 22 Consumption of sea slugs by scleractinian corals island supporting large populations of free-living mushroom corals [41±43]. Beyond the reef slope there is a soft-sediment ecosystem that supports mixed aggregations of free-living scler- actinian corals such as Heteropsammia cochlea and Heterocyathus aequicostatus [26,31]. This ecosystem has been shown to support a hidden diversity of sea slugs and other fauna that are not present within the shallower reef habitats, with over a third of all species of sea slug recorded from the island exclusively recorded from this ecosystem [44, 45]. To date, seven spe- cies of sacoglossan sea slug are known from Koh Tao [44], including two species of Plakobran- chus. The recent description of Plakobranchus papua [45] has helped identify a third cryptic species living in sympatry with Plakobranchus cf. ocellatus at Koh Tao, herein referred to as Plakobranchus
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